Skip to main content
Log in

The effect of trematode infection on the markers of oxidative stress in the offspring of the freshwater snail Lymnaea stagnalis

  • Immunology and Host-Parasite Interactions - Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Most invertebrate species exhibit immunological responses that can inactivate and eliminate penetrating parasites. Such immune responses in particular involve the formation of potentially toxic reactive oxygen species (ROS). We explored the immune capabilities of the first-generation (F1) offspring of naturally infected freshwater snails, Lymnaea stagnalis, in response to infection by trematode cercariae under laboratory conditions. The rates of ROS formation and peroxidase activity in the hemolymph of the F1 offspring of L. stagnalis parents infected by an asexual stage of trematodes were significantly higher than in F1 offspring of uninfected parents. Compared to offspring from uninfected parents, the growth rate of F1 snails from infected parents was higher, but survival was lower. After infection of F1 snails by trematode cercariae of Echinoparyphium aconiatum under laboratory conditions, the rate of ROS formation and peroxidase activity in the hemolymph of F1 offspring of uninfected parents increased compared to control snails. This pattern persisted throughout the entire 3-week observation period. In contrast, the rate of ROS formation in the hemolymph of F1 snails from infected parents after experimental infection by E. aconiatum cercariae did not differ from controls, and peroxidase activity even decreased. Thus, trematode parthenitae infection of parents could alter the immune response of their offspring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Arakawa T (1994) Superoxide generation in vitro in Lepidopteran larval haemolymph. J Insect Physiol 40:165–117

    Article  Google Scholar 

  • Ataev GL (2010) The influence of Echinostoma caproni metacercariae (Trematoda) on the survival of biomphalaria molluscs (Pulmonata). Parasitologiia 44:481–495

    CAS  Google Scholar 

  • Chambers MC, Schneider DS (2012) Pioneering immunology: insect style. Curr Opin Immunol 24:10–14

    Article  CAS  Google Scholar 

  • Dikkeboom R, van der Knaap WPW, Mueleman EA, Sminia T (1984) Differences between blood cells of juvenile and adult specimens of the pond snail Lymnaea stagnalis. Cell Tissue Res 238:43–47

    Article  Google Scholar 

  • Dordrecht Gornowicz D, Dmochowska K, Zbikowska E, Zoltowska K (2013) Total antioxidative status and the activity of peroxidase and superoxide dismutase in the haemolymph of Lymnaea stagnalis (L.) naturally infected with digenean trematodes. J Mollusc Stud 79:225–229

    Article  Google Scholar 

  • Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes. Kluwer Academic Publishers

  • Krasnolobova TA (1987) Trematodes of fauna (animals) of USSR. Plagiorchis genus. Nauka Press, Moscow

    Google Scholar 

  • Little TJ, O’Connor B, Colegrave N, Watt K, Read AF (2003) Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13:489–492

    Article  CAS  Google Scholar 

  • Milutinovic B, Kurtz J (2016) Immune memory in invertebrates. Semin Immunol 28:328–342

    Article  CAS  Google Scholar 

  • Moné Y, Ribou A-C, Cosseau C, Duval D, Théron A, Mitta G, Gourbal B (2011) An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions. Int J Parasitol 41:721–730

    Article  Google Scholar 

  • Moret Y, Schmid-Hempel P (2001) Immune defence in bumble-bee offspring. Nature 414:506

    Article  CAS  Google Scholar 

  • Nappi AJ, Ottaviani E (2000) Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22:469–480

    Article  CAS  Google Scholar 

  • Nicell JA, Wright A (1997) A model of peroxidase activity with inhibition by hydrogen peroxide. Enzym Microb Technol 21:302–310

    Article  CAS  Google Scholar 

  • Ottaviani E (2015) Invertebrate immunological memory: could the epigenetic changes play the part of lymphocytes? Invertebr Surviv J 12:1–4

    Google Scholar 

  • Slepneva IA, Glupov VV, Sergeeva SV, Khramtsov VV (1999) EPR detection of reactive oxygen species in haemolymph of Galleria mellonella and Dendrolimus superans sibiricus (Lepidoptera) larvae. Biochem Biophys Res Commun 264:212–215

    Article  CAS  Google Scholar 

  • Sminia T (1972) Structure and function of blood and connective tissue cells of the freshwater pulmonate Lymnaea stagnalis studied by electron microscopy and enzyme histochemistry. Z Zellforsch Mikrosk Anat 130:497–526

    Article  CAS  Google Scholar 

  • van der Knaap WPW, Adema CM, Sminia T (1993) Invertebrate blood cells: morphological and functional aspects of the haemocytes in the pond snail Lymnaea stagnalis. Comp Haematol Int 3:20–26

    Article  Google Scholar 

  • Vilcinskas A (2016) The role of epigenetics in host–parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum. Zoology 119:273–280

    Article  Google Scholar 

  • Vorontsova YL, Slepneva IA, Yurlova NI, Glupov VV (2015) Do snails Lymnaea stagnalis have phenoloxidase activity in hemolymph? Invertebr Surviv J 12:5–12

    Google Scholar 

  • Yurlova NI, Vodyanitskaya SN, Serbina EA, Biserkov VY, Georgiev BB, Chipev NH (2006) Temporal variation in prevalence and abundance of metacercariae in the pulmonate snail Lymnaea stagnalis in Chany Lake, West Siberia, Russia: long-term patterns and environmental covariates. J Parasitol 92:249–259

    Article  Google Scholar 

Download references

Funding

The study was supported by The Federal Fundamental Scientific Research Programme for 2013-2020 (АААА-А16-116121410124-8) and AAAA-A18-1181222190010-8.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yana L. Vorontsova.

Additional information

Handling Editor: Julia Walochnik

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vorontsova, Y.L., Slepneva, I.A., Yurlova, N.I. et al. The effect of trematode infection on the markers of oxidative stress in the offspring of the freshwater snail Lymnaea stagnalis. Parasitol Res 118, 3561–3564 (2019). https://doi.org/10.1007/s00436-019-06494-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06494-5

Keywords

Navigation